Durham Research Online
Deposited in DRO:
16 March 2016
Version of attached le:
Published Version
Peer-review status of attached le:
Peer-reviewed
Citation for published item:
Attwell, L. and Kovarovic, K. and Kendal, J.R. (2015) 'Fire in the Plio-Pleistocene : the functions of hominin
re use, and the mechanistic, developmental and evolutionary consequences.', Journal of anthropological
sciences., 93 . pp. 1-20.
Further information on publisher's website:
http://www.isita-org.com/jass/Contents/ContentsVol93.htm
Publisher's copyright statement:
This paper is available under the terms of a Creative Commons Attribution-NonCommercial 4.0 Unported License.
Additional information:
Use policy
The full-text may be used and/or reproduced, and given to third parties in any format or medium, without prior permission or charge, for
personal research or study, educational, or not-for-prot purposes provided that:
• a full bibliographic reference is made to the original source
• a link is made to the metadata record in DRO
• the full-text is not changed in any way
The full-text must not be sold in any format or medium without the formal permission of the copyright holders.
Please consult the full DRO policy for further details.
Durham University Library, Stockton Road, Durham DH1 3LY, United Kingdom
Tel : +44 (0)191 334 3042 | Fax : +44 (0)191 334 2971
http://dro.dur.ac.uk
JASs Invited Reviews
doi 10.4436/jass.93006
Journal of Anthropological Sciences
Vol. 93 (2015), pp. 1-20
Fire in the Plio-Pleistocene: the functions of hominin
fire use, and the mechanistic, developmental and
evolutionary consequences
Laura Attwell1, Kris Kovarovic1 & Jeremy R. Kendal1,2
1) Department of Anthropology, Durham University, South Road, Durham DH1 2SJ, United Kingdom
e-mail: [email protected]
2) Centre for the Coevolution of Biology and Culture, Durham University, Durham DH1 2SJ, United
Kingdom
Summary - Fire is a powerful natural force that can change landscapes extremely quickly. Hominins
have harnessed this resource for their own purposes, with mechanistic and developmental physiological
consequences. In addition, the use of fire has niche constructive effects, altering selective environments for
genetic and cultural evolution. We review the record for hominin fire use in the Plio-Pleistocene, before
considering the various functions for its use, and the resultant mechanistic and developmental consequences.
We also adopt the niche construction framework to consider how the use of fire can modify selective
environments, and thus have evolutionary consequences at genetic and cultural levels. The light that fire
produces may influence photoperiodicity and alter hormonally-controlled bodily rhythms. Fire used for
cooking could have extended the range of foods hominins were able to consume, and reduced digestion costs.
This may have contributed to the expansion of the hominin brain and facial anatomy, influenced by a higher
quality cooked diet. Fire may also have allowed dispersal into northern areas with much cooler climates than
the hominin African origin, posing novel problems that affected diet and social behaviours.
Keywords - Fire, Photoperiodicity, Hominin dispersal, Social evolution, Cooking, Niche construction.
Introduction
The use and control of fire is considered one
of the most significant innovations in the evolution of modern human behaviour. Harnessing
the warmth and light provided by burning fires
has wide-ranging implications for our ancestors’ lifestyles, from opening up new avenues for
food preparation via cooking, to providing safety
from predators, and extending the visible part of
the day during which tasks could be safety conducted. The implications may be physiological
and morphological as well as behavioural; for
example, changes in the dietary resources that
can be exploited will have an effect on the digestive process of energy extraction and the masticatory architecture responsible for processing the
food. Toxins found in campfire smoke, which
may accumulate in the placenta during pregnancy, have even been suggested to account for
the lack of placentophagy in humans, a homoplastic trait unique only to extant camelids and
ourselves (Young et al., 2012).
Fire is a naturally occurring process, having
long played a key role in ecosystem composition
and maintenance on a global scale (Scott, 2000;
Bond et al., 2005; Thevenon et al., 2010; Pausas
& Keeley, 2009). It can be responsible for clearing old growth and encouraging new, dispersing
seeds and maintaining open patches in otherwise
closed habitats (Kerr et al. 1999; Bond & Keely,
2005). The savanna mosaics and dry forests of
Africa where early hominins evolved, characterised by an increasing amount of flammable C4
the JASs is published by the Istituto Italiano di Antropologia
www.isita-org.com
2
Functions and consequences of hominin fire use
grasslands provided the perfect conditions for
natural wildfires (Menault, 1983; Gichohi et
al., 1996; Bobe, 2006; Pausas & Keeley, 2009).
Palaeosedimentary records trace the existence of
these natural fires through charred grass cuticles
in Africa from the Late Miocene onwards, corresponding to the emergence of both C4 grasslands
and the hominin lineage (Morely & Richards,
1993; Jacobs, 2004).
It is reasonable to surmise that early hominins would have come into contact with fire as
often as the other mammals in their Pliocene and
Pleistocene communities. This familiarity would
certainly be the necessary precondition for any
emergent behaviour in which fire is approached
and its possible uses eventually ascertained.
Anecdotal observational evidence suggests that
this basic familiarity may be accompanied by
the ability to infer the movement of natural fires
and alter behaviour accordingly in extant chimpanzees, our closest living relatives, in Fongoli,
Senegal (Preutz & LaDuke, 2010). If living
apes are indeed good models for reconstructing
the behavioural repertoire of our earliest ancestors, there is no reason to believe that hominins
would have been anything but familiar with
and able to adapt to the movement of natural
fires. However, this behaviour evolved over the
past 6-8 million years to encompass not simply a
conscious awareness of natural fires, but the cognitive capability to learn what its light and heat
could be useful for and the knowledge of how
fires could be maintained over time when they
occurred naturally.
A major phase shift seems to have occurred
after 1 million years ago, when archaeological
evidence indicating that hominins developed the
ability to ignite their own fires begins to mount
(e.g. Goren-Inbar et al., 2004; Berna et al., 2012).
Hominins thus became a part of the natural fire
regime, representing an additional source of ignition (i.e to lighting strikes, etc; Archibald, et al.,
2012). At this point, the ability of hominins to
shape their own environments through the use
of fire increased significantly. It is thought that
the peak of human-driven burning in Africa
occurred between 4,000 and 40,000 years ago
(Archibald et al., 2012), but both its historical
and current utility in many societies, who transform landscapes for agricultural and other purposes, is undeniable.
Our review sets out the record for hominin
fire use in the Plio-Pleistocene, before considering mechanistic and developmental responses,
in addition to evolutionary consequences of fire
use. The latter considers both changes in biological and cultural evolutionary trajectories,
which can be conceptualised together using a
niche construction framework. Niche construction refers to the modification that organisms
make to their environments (Odling-Smee et
al., 2003) and offers a convenient way of tracing
the complex causal interactions between evolving genetic and cultural variation over hominin
history. Key aspects of this framework include
explicit accounting for the effects of ontogenetic
processes, including hormonal change and social
learning, on the selective environment, and also
the ecological inheritance of modified environments across generations (see Fig. 1).
A unique feature of hominin evolution is
likely to have been the high degree of cultural
niche construction, for instance, as human species altered and constructed their own environments through cumulative cultural evolution
of technology and social normative systems
(Richerson et al., 2010). This process caused
rapid qualitative change in the selective environments of both human genes, as well as affecting
cultural evolutionary dynamics (Odling-Smee
et al., 2003; Laland et al., 2010). As an illustration of this relationship between human behaviour and biological change, we speculate that the
use of fire for cooking, which kills many of the
harmful pathogens present in raw meat1, potentially relaxed genetic selection for resistance to
meat-borne pathogens. Similarly, the use of
fire and clothing counteracts exposure to variation in environmental temperature, dampening
1
Although focussing on the relationship between meateating and longevity in humans, Finch & Stanford
(2010) provide a useful summary of the pathogens
found in animal organs which may have been encountered by early hominins exploiting animal resources.
L. Attwell et al.
3
Fig.1 - Cultural niche construction can alter the selective environment to affect cultural evolution
(route 1) or, in the absence of a cultural response, to affect genetic evolution (route 2). The resultant genetic evolutionary change can feed back to affect further cultural change. Figure redrawn
from Odling-Smee et al. (2003).
selection for genes favoured for hot or cold climates (Laland et al., 2010). Figure 1, redrawn
from Odling-Smee et al. (2003), illustrates that
cultural niche construction, such as the use of
fire facilitating the migration to cold climates,
may result in cultural evolution (route 1), such as
the use of warm clothing. To some degree however, the cultural evolution of technology may
not counteract exposure to the cold, resulting
in the opportunity for genetic evolution over a
longer time scale (route 2), such as the reduction
in limb length as posited by Allen’s rule (1877).
Early record of hominin fire use
Past fires may be evidenced by layers or lenses
of ash, charcoal and the charred remains of vegetation or bone. The determination of hominincontrolled or hominin-ignited fires versus those
which have occurred without their involvement
(for instance, lightning or volcanic activity)
relies on being able to calculate the temperature
at which a fire has burned, the effect it had on
localised sediments and the type and extent of
chemical changes that have occurred in bone
exposed to heat. Intentionally controlled fires
tend to burn longer and at higher temperatures,
the effects of which are particularly noticeable at
sites that have been used on multiple occasions,
such as hearths (e.g. Bellomo, 1993; Preece et al.,
2006; Goren-Inbar et al., 2004). Problematically,
there is little that can be done to identify naturally occurring fires that may have been utilised
by hominins as and when they occurred prior to
their ability to control it even for a short period
of time. For example, tree stump fires occur naturally and leave little trace but may have been
used opportunistically as cooking fires (Bellomo,
1994). This early stage in our relationship with
fire is therefore nearly impossible to reconstruct
and remains highly speculative.
Wonderwerk Cave in South Africa has a long
history into the investigation of hominin controlled fire use (Fig. 2). Evidence of fire can be
seen throughout most of the sequence, but of
greatest interest to the evolution of fire use are
the burnt bones and plants present throughout
the entirety of the Acheulean occupied Stratum
10, which has recently been dated to 1 mya
(Berna et al., 2012). The consistent pattern of
burnt remains is suggestive of intentional and
www.isita-org.com
4
Functions and consequences of hominin fire use
continued fire use; in one excavated unit, 80%
of the bone sample displayed discolouration
typical of burning. Fourier transform infrared
microspectroscopy analysis of the remains concludes that fires reached no higher than 700°C,
consistent with light plant vegetation, such as
leaves and grasses, as fuel. Numerous researchers
(see Beaumont, 2011 for a review and references
therein) had previously postulated that ash and
an extremely high frequency of small charred
bone remains in the excavated areas of Major
Unit 9b, signified fire use by approximately 1.7
mya, even estimating that the 1 m3 volume of
ash was formed through the burning of at least
3,000 night-long fires, each requiring 5kg of
woody fuel. The distribution of ash within the
unit is also argued to be consistent with a home
base type of living situation, supporting the idea
of a band of hominins living and communicating
together inside the cave. Although the presence
of associated Acheulean deposits in Stratum 10
makes it reasonable to conclude a relationship
between the burning and hominin occupation,
the earlier estimated date of 1.7 mya for this level
is likely to have been incorrect. Earlier Oldowan
strata do date to this time, but evidence for the
presence of fire there is inconclusive (Chazan et
al., 2008). Member 3 of Swartkrans Cave, further north in the Cradle of Humankind cluster
of sites, has also been suggested as the earliest
instance of southern African controlled fire at 1.5
mya by developed Oldowan hominins (Brain,
1993; Sillen & Hoering, 1993; Brain & Sillen,
1988). A relatively small proportion of flint artefacts do appear to have reached reasonably high
temperatures, but the context of this material is
unclear (Brain, 1993). Many find it difficult to
accept an association between the burnt remains
and hominins, the most abundant species from
Member 3 being the robust australopithecine
Paranthropus robustus (Pickering, 2001).
The earliest, although highly contested, evidence of hominin fire use in East Africa dates to
1.6 mya at Koobi Fora, Kenya, on the eastern
shores of Lake Turkana. Here some of the most
frequently cited early oxidised sediment studies
and spatial analyses were applied specifically to
substantiate the presence of hominin-induced
fire (Bellomo, 1991, 1993, 1994; Bellomo &
Kean, 1994). Numerous lithic artefacts were
uncovered during early phases of research at the
site (Harris, 1978) and subsequently two oxidised
features of unknown origin were identified in
one of the main excavated areas. Although there
is no evidence that the lithic tools from either
oxidised feature were intentionally burned, their
distributions around one of the features indicates
some association, assumed to be behavioural
rather than taphonomic (Bellomo, 1994). The
lack of both charred tools and boney remains
indicates that the fires had no role in preparing
lithic resources for manufacture or food processing for consumption. However, sedimentation
studies infer that a campfire had been lit and
maintained over a period of several days and
the spatial analyses suggest that the fire served
as a focal point around which tools were created
(Bellomo, 1994). They represent the distinctive
Karari Industry, an early Acheulean tool type
restricted to the Koobi Fora region between 1.65
and 1.39 mya (Brown, 1994) and thought to be
associated with the arrival of the hominin species
now referred to as Homo ergaster.
Additional early East African evidence is
even more scant than at Koobi Fora. It includes
some evidence of burnt clay further south at
Chesowanja, near Lake Baringo, which is said
to be caused by longer-term burns than a natural fire would allow (Gowlett et al., 1981) and
the Ethiopian site of Gadeb and other isolated
Middle Awash localities (Barbetti et al., 1980;
Clark & Harris, 1985) where burnt rocks have
been reported. These sites collectively do not
make the most convincing case, but some have
argued that they represent an early phase of
a technological transition associated with the
Acheulean hominin, Homo ergaster (e.g. Clark &
Harris, 1985; Clark, 1987).
It is not until well into the Pleistocene that evidence for the use of fire by hominins becomes more
widely accepted. The earliest of these sites is Gesher
Benot Ya’aqov in Israel, a lake margin site dated to
790 kya (Goren-Inbar et al., 2000: Goren-Inbar
et al., 2002, 2004; Alperson-Afil & Goren-Inbar,
L. Attwell et al.
5
Fig. 2 - A map of Plio-Pleistocene sites in Africa, Asia and Europe where evidence for hominin use
of fire is known in each region. Only sites mentioned in this review are shown. Dates are taken
from the following sources: Gowlett et al., 1981; Clark & Harris, 1985; Brain, 1993; Bellomo & Kean
1994; Mercier et al., 2004; Rolland, 2004; Thieme, 2005; Mania & Mania, 2005; Preece et al., 2006;
Arzarello et al., 2007; Karkanas et al., 2007; Carbonell et al., 2008; Richter et al., 2008; Alperson-Afil
& Goren-Inbar, 2010; Berna et al., 2012; Peris et al., 2012.
2006; Alperson-Afil et al., 2007; Alperson-Afil &
Goren-Inbar, 2010). Thermoluminescence analysis indicates that wood and flint artefacts were
burnt continuously during the 100,000 year occupation, and the distribution of the lithics further
suggests burning in specific areas, as would be the
case in a hearth-like arrangement (Alperson-Afil
& Goren-Inbar, 2010; Alperson-Afil et al., 2007).
It is unlikely that natural fires are responsible for
the thermal damage or spatial patterns of artefacts
found at the site; the frequency of burnt organic
materials, including presumed food items, are not
high enough to be attributed to natural wildfire
and the repetitive nature of fire over such a long
time period further infers that hominins were able
to ignite and maintain it themselves without harvesting flames from natural sources (Goren-Inbar
et al., 2004; Alperson-Afil, 2008; Alperson-Afil &
Goren-Inbar, 2010). The hominin species responsible for the fires at this site in this time period
remains unknown, but other evidence suggests
that the Acheulean tool-making inhabitants of the
area hunted, processed meat, gathered plant foods,
extracted bone marrow, quarried multiple lithic
resources, created tools and kindled fire effectively
(Goren-Inbar et al., 2000, 2002). Others argue
that fire was not a significant aspect of Levantine
hominin lifeways until approximately 400-200
kya, as evidenced by wood ash and numerous
associated burnt mammal remains Qesem Cave
(e.g. Karkanas et al., 2007)
If the date from Qesem Cave is accepted as
evidence that hominins did not control fire in the
corridor between Africa and Asia until around
400 kya, this behaviour must have evolved independently in Asia if fire use at Zhoukoudian,
www.isita-org.com
6
Functions and consequences of hominin fire use
China, at 780-680 kya is correct (Rolland, 2004).
Evidence at Zhoukoudian includes charred mammal bones and burnt hackberry shells, lithics and
eggshell flakes. The processing of these materials
is likely to have been performed by Homo erectus, the remains of which have also been uncovered in the same layers (Rolland, 2004). Some
mammal remains appear to have been burnt as
fresh bone and other remains bear tool-induced
cut marks, suggestive of scavenging aided by fire
(Boaz et al., 2004). However, fire within these
caves cannot be conclusively attributed to hominin activity. Although hominin occupation is
likely, many of the bones, both hominin and
non-hominin mammal, bear traces of carnivore
tooth marks; this and other evidence points to
occupation by large carnivores during this time
(Boaz et al., 2000). There is also no trace of ash
or charcoal at the site suggesting natural causes
are at the root of the fire (Weiner et al., 1998).
In Europe the evidence for fire is clearer,
though it confuses the story of hominin occupation in Europe. Homo made it to Europe
1.2 - 1.1 mya (Carbonell et al., 2008), if not
much earlier in limited numbers (if the dates
are correct from Pirro Nord in Italy) by 1.7 mya
(Arzarello et al., 2007). However, fire control
evidence is dated to only 400 kya (e.g. Preece et
al., 2006, 2007; Richter et al., 2008) (see Fig.
2). The much more recent date for fire control
compared to the initial hominin occupation suggests that early populations survived in Europe
without the use of fire for an extended period
of time (Roebroeks & Villa, 2011). For example,
at Beeches Pit in Suffolk, UK, evidence dated to
400 kya includes burnt flints, charred and calcified bones and burnt sediments (Preece et al.,
2006). The distribution of artefacts suggests a
hearth-like arrangement in which the fire was the
centre around which focused activities such as
tool making would occur. Elsewhere in northern
Europe, at Menez-Dregan in France, evidence
has been found of controlled fire dated to 200
kya in layers 5c and e, and potentially evidence
from 400 kya in layer 9 (Mercier et al., 2004). In
Germany, evidence of domesticated fire dated to
400 kya has been found at Schöningen (Thieme,
2005) and also at Bilzingsleben around 370 kya
(Mania & Mania, 2005). More recent evidence
at Bolomor Cave, Spain has been dated to 230
kya (Peris et al., 2012). The evidence of hearths
here shows that the fires were not of long duration, and were not repeated at exactly the same
points. The time between each fire varied and
the characteristics of the area suggest they were
used for subsistence. This is currently the earliest
evidence of controlled fire in Southern Europe.
Function and consequences of fire use
There are a myriad of ways in which the use
and eventual control of fire may have impacted
upon hominin biology and culture. We consider
below the most relevant, direct effects and evidence in support of them.
Photoperiodicity
Here we focus on the developmental effects of
light on photoperiodicity and consider Burton’s
(2009) assertion that firelight, by extending
daylight hours, may have physiological consequences for daily and annual cycles. We consider
such claims worthy of mention although with
caution and in the spirit of interesting conjecture, until preliminary evidence is substantiated.
Photoperiodicity is the response of organisms to the length of exposure to daylight and
allows organisms to synchronise seasonal and
daily activities according to the duration of
daylight hours as a function of the earth’s rotation. This has important implications for timing
certain behaviours, such as reproduction, to the
most appropriate part of the year (Kuller, 2002).
For example, it is particularly advantageous to
ensure there will be enough food available at
metabolically expensive periods of reproduction,
whether that is gestation or lactation, to increase
the chance of offspring survival. This is especially
important for seasonal breeders, including many
primates such as the lesser mouse lemur, whose
breeding season occurs only after the shortest day
of the year. As daylight hours increase, females
come into oestrus, male testicles increase in size,
L. Attwell et al.
and offspring are eventually born in the rainy
seasons of their native Madagascar when food
is most abundant (Glatstone, 1979). Indeed,
dietary restrictions are generally considered to be
the ultimate reason for the seasonal regulation of
birthing cycles in primates (Doran, 1997), with
photoperiod being the proximate explanation
(Lindburgh, 1987; Wehr, 2001; Tsantarliotou &
Taitzoglou, 2012). However, even non-seasonal
breeders show a peak in conceptions coinciding with food abundance for either gestation
or lactation (Brockman, 2005; Tsantarliotou &
Taitzoglou, 2012) and limited experimental evidence suggests this is also the case in humans and
other apes, with chimpanzees known to resume
postpartum cycles during the dry season in preparation for conceptions and birth later in the
year when food scarcity has decreased with the
onset of the more abundant, wet season (Wallis,
1995, 1997; Wehr, 2001). Studies of humans are
clouded by multiple confounding factors including cultural differences and attitudes towards
reproduction, but it is known that some females
vary in their seasonal reproductive responses
much more than others, and that this may be a
heritable characteristic (Wehr, 2001).
Light is important in cueing daily activity
patterns and circadian clocks. In humans, the
suprachiasmatic nucleus in the hypothalamus
controls daily oscillations (Stehle et al., 2003)
such as red blood cell turnover, heart rate, sleep/
wake cycles and hormone levels. While the 24
hour cycle is “built in” to many animals (Gorman
& Lee, 2002), sunrise and sunset act as reference
points for these cycles and shifts in these reference points may cause concomitant shifts in daily
rhythms. In humans and apes, photoreceptor
cells in the eye are responsible for sensing light
and converting it into chemical substances, such
as the pigment melanopsin, which acts on the
pineal gland in the brain (Sancar, 2000, 2004;
Cashmore, 2003). Melatonin, the only known
hormone to be secreted by the pineal gland, is
heavily influenced by the amount light detected
by the eyes. Light suppresses its production, so
that the peak is typically two hours after nightfall
(Brainard et al., 2001; Goldman, 2001).
7
Melatonin has a number of effects throughout the body2, one of which is on the pituitary
gland, which controls all other endocrine glands
in the body; it therefore has an effect on all
aspects of homeostasis that are controlled by hormones, and particularly reproduction through an
extremely complex hormonal cascade. Melatonin
influences a number of points within the cascade, all of which have implications for the onset
of puberty. Studies have found that exposure to
differing levels of melatonin can induce puberty
in seasonal breeders such as rhesus monkeys,
whose onset is known to be triggered by short
day length (Wilson & Gordon, 1989; Wilson et
al., 1988). Prepubertal rhesus monkeys injected
with melatonin, which has the effect of lengthening the natural night-time rise in melatonin,
reach puberty earlier than those not receiving
the injections (Wilson & Gordon, 1989a). In
humans, longer daylight hours can reduce the
age of menarche (Dossus et al., 2013).
Melatonin also induces sleep (Cajochen et al.,
2003) and a lack of it can result in sleeping disorder or a change in sleeping pattern (e.g. Ried
& Zee, 2005; Dumont & Beaulieu, 2007). Along
with a change in sleeping pattern, changes in light
exposure and melatonin levels can have negative effects. For example, a change in the timing
of the biological clock, as a result of changes in
melatonin levels that does not correspond to daily
activities, is known to be the main cause of circadian sleep disorders (Reid & Zee, 2005). Seasonal
affective disorder (SAD) has also been related to
light exposure, with higher than normal melatonin levels believed to be a contributory factor
(Rosenthal et al., 1984; Wehr et al., 2001).
Burton (2009) considered the possible impact
of fire on hominin physiology and development
by speculating on the possible impact of reduced
2
Although not the focus of this review, there is increasing
medical evidence that bed-time supplements of melatonin can lower the blood pressure of nocturnal hypertension patients, reducing their risk of numerous cardiovascular problems. The exact mechanism for this has not
been determined, but the role of melatonin in regulating more than sleep cycles during the night is becoming
clear (see, for example, Grossman et al., 2006, 2011)
www.isita-org.com
8
Functions and consequences of hominin fire use
melatonin production caused by exposure to firelight in modern humans, which may have shifted
the body clock. Blue light (446-477nm) has the
greatest effect on human circadian rhythms
(Lockley et al., 2003), with only 1.5 hours of
exposure being enough to shift the body clock
by 3 hours (though the intensity of light is also
important). Blue light is found at the base of
a flame, and only 1.3 lux of light is required to
affect melatonin levels in humans (Raloff, 1998).
But is the light from a fire enough to have caused
a physiological effect in hominins? Burton’s
(2009) preliminary experimentation suggests
that the lux entering the eye in various positions
and distances from a campfire would range from
3-50 lux, though only if the gaze was trained
towards the base of the campfire. She speculates
that even at the lower end of the range, firelight
may have had an effect on melatonin levels,
since as little as 5 lux can suppress production
(Lockley et al., 2003). Thus, although empirical
support demonstrating that fire-induced hormonal effects occurred in our evolutionary past is
lacking, it would appear feasible that the effects
of firelight on melatonin could have contributed
to a phase shift in sleep patterns in addition to
the timing of puberty. A recent study also demonstrated in humans that exposure to light suppressed uterine contractions during night-time
labour, with melatonin decreases implicated in
the delay of parturition (Olcese et al., 2013).
While fire may have hormonally-mediated
photoperiodic effects, it is not clear that the
proposed photoperiodic changes have evolved
under natural selection, rather than simply
being a plastic developmental response to modification of the environment. However, there is
mounting evidence from small mammals, such
as hamsters, and a variety of insect species that
strongly suggests photoperiod timing is passed
to the next generation during foetal development through maternal melatonin secretion
patterns (Goldman, 2003), but this has not yet
been demonstrated in humans (Wehr, 2001). In
addition to this heritable component, photoperiodic changes may well have provided hominins
with a novel temporal niche affecting the cultural
evolution of traditional hours for activities such
as sleeping, or facilitated the evolution of norms
for social interaction and information exchange
around the camp fire.
Social evolution
The warmth and light of a camp fire would
provide a natural focal point for social gathering in safety from predators (Rolland, 2004). As
Stiner et al. (2010, p. 230) say, “sheltered spaces
are intensely social spaces” and, as such, may
have created new selective conditions for both
the genetic and cultural evolution underpinning
hominin sociality.
The social brain hypothesis is particularly
relevant, suggesting that hominin brain size
evolved as a result of demanding social environments, such as large group size. In order to keep
track of all the members of a group and manage relationships within it, an individual would
require a larger brain to process information
concerning identity, reputation and allegiances
(Dunbar, 1998). There are a number of cognitive implications that maintaining a fire has on
the brain related to both group sharing and the
specific provisioning of the fire (we refer the
reader to an extensive review by Twomey (2013)
for details). A fire would be too demanding for
a single individual to care for and protect alone,
so the maintenance of a flame requires withingroup co-operation or significant power differential and enforcement. If a public good, no
one individual would own or use the fire, while
many would have access to it and work to keep
it alight. This form of cooperation may require
understanding of a shared goal, the capacity to
arrange the division of labour and cooperative
planning to ensure continuation of the flame, for
example collecting fuel or protecting the flame
(Tomasello, 2009; Twomey, 2013). As Twomey
notes (2013, p. 114), these capacities may rely on
cognitive facilities such as “informational theory
of mind, joint attention, collective intentionality
and intersubjective communication”.
Also important would be the communications between groups, because inevitably flames
go out from time to time. Evidence such as that
L. Attwell et al.
from Beeches Pit, Suffolk, UK (Fig. 2), suggests that even at 400 kya, fire could not be
intentionally kindled and therefore needed to
be maintained over long periods of time (Preece
et al., 2006). If so, fire may have been collected
from neighbours once a group’s own source had
gone out, thus affecting the development of
between-group social networks (Gamble, 1999).
The longer term ties between groups would
have required a large memory store to be able
to remember individuals within another group.
It would have also required the ability to put
value to items if receiving the source of a flame
was achieved by trade. Together, these cognitive
challenges may have contributed to the major
increase in brain size observed at 400-200 kya
(Shultz et al., 2012), consistent with the timing
for the regular, habitual use of fire.
Dispersal
Northward dispersal of hominins into cooler,
more temperate climates, and survival during
glacial periods in Europe, are both likely to have
intensified the selective advantage of fire use
(Gamble, 1999; Gowlett, 2006). Gowlett (2006)
suggests that when northern areas were occupied,
the utilisation of fire must have been necessary,
for example, in thawing food (Brace 1999) or
maintaining warmth while sleeping (Wrangham
& Carmody, 2010).
However, the archaeological record does not
clarify whether the timing of dispersal into Eurasia
from Africa, or to colder, more seasonal parts of
Europe and Asia by existing populations occurred
before or after fire was actively used by these
migrant hominins. Although the Levantine sites of
Gesher Benot Ya’aqov (Goren-Inbar et al., 2004)
and Qesem Cave (e.g. Karkanas et al., 2007) show
that fire was likely used along the most obvious
migratory route between Africa and the rest of
the Old World during the Middle Pleistocene,
dates from the earliest fire-related sites in Asia (i.e.
Zhoukoudian 780-680 kya; Rolland, 2004), and
Europe (approximately 400 kya; e.g. Preece et al.,
2006, 2007; Richter et al., 2008) do not accord
with the idea that fire simply accompanied the
first waves of hominins leaving Africa and was
9
maintained as a tradition. There is no evidence,
for example, of fire use at 1.8 mya at Dmanisi,
Georgia, which is likely to represent one of the first
populations that migrated from Africa (Gabunia et
al., 2000). The late arrival of fire use in Europe
and the apparently simultaneous emergence of this
behaviour in Asia and the Levant relative to the
arrival of hominins suggest three possible scenarios: 1) fire did not accompany the first migratory
populations and this behaviour evolved in Europe
and Asia in situ at different times or 2) fire accompanied the first migratory populations but the skill
was either forgotten or practiced so ephemerally
that it left no observable trace or 3) fire accompanied the first migratory populations but they are
not represented in the Levantine record despite
having moved through the area or because they
took another route. None of these scenarios can be
substantiated at present, although it has been postulated that the mis-match between the distribution and timing of the evidence in comparison to
the presence of hominins is likely to indicate that
the use of fire did in fact develop independently in
multiple locales (e.g. Roebroeks & Villa, 2011).
Thus, it is possible that sustained living in northerly climates contributed to the cultural evolution
of controlled fire use rather than knowledge of fire
facilitating initial movement into these latitudes.
If that is the case, and hominins were able to innovate the use of fire for heat protection against the
cold, a form of counteractive niche construction,
it may have allowed them to continue surviving in
the areas they had already occupied.
The ecological data from Europe makes it particularly difficult to reconcile the lack of fire with
hominin success in this region. Europe experienced repeated glaciations during the Pleistocene,
resulting in climate fluctuations and concomitant
changes in ecosystems. But, it is possible that early
hominin populations first arrived and thrived in
northern Europe during an interglacial period
with a relatively mild climate, so that fire was not
a necessity (Gowlett, 2001). Once a glaciation
event began to reduce the temperature and cover
northern Europe with an ice sheet, these cold
temperatures of glacial periods, regularly below
0°C, would have posed significant problems for
www.isita-org.com
10
Functions and consequences of hominin fire use
hominins in maintaining body temperature and
collecting food and other resources. Selective pressures to develop fire control may have acted on
these early populations. This homeostatic use of
fire is a form of counteractive niche construction,
by buffering against selection pressure imposed
by exposure to cold temperatures (Odling Smee
et al., 2003). However, the warmth of fire would
have only partially reduced exposure to the external environment, thus by contributing to the persistence of populations living in northern climes,
fire use is likely to have affected genetic and cultural evolutionary adaptations to cold climes. For
example, the cultural practise of wearing clothes
may have been influenced by the necessity to keep
warm and certainly there are tools in the archaeological record that were likely to have been utilised
in the preparation of hides (i.e. scrapers), which
are thought to have been used by Neanderthals
and earlier taxa by approximately 780 kya in
Europe (Carbonell et al., 1999). However, evidence for the hides themselves is obviously lacking. Genetic evidence for the initial emergence of
modern human clothing lice further suggests that
the use of clothing was an established behaviour
by 170 kya, correlating to the onset of an ice age
in Europe (Toups et al., 2011). This suggests that
the technology necessary for the creation of items
that would protect against the increasingly colder
temperatures may have contributed to the success
of modern humans when they migrated out of
Africa. The “modern” cultural behaviours attributed to Homo sapiens, including the production of
better adapted and more complex clothing as evidenced by tools that would facilitate their production (i.e. needles), are commonly understood to
have contributed to the success of this species over
Neanderthals once their populations were established in Europe and following their prolonged
sympatric existence of two to five thousand years
in some areas (Higham et al., 2014).
Cooking
Heat is a significant product of fire that
may have had an evolutionary effect on hominins through its use in cooking, which will
have enhanced the digestion and palatability
of animal foods, resulting in a higher energy
and quality diet, and mitigated the effects of
the toxic and digestion-inhibiting substances
found in many plants and tubers (Wrangham &
Carmody, 2010). Overall, the effect would likely
be a broadening of the dietary niche exploited
by the populations that engaged in fire-assisted
processing of resources, consequently changing
selection pressures acting on the hominin digestive and masticatory systems.
Diverse and primarily vegetation-based diets
are well-documented in early hominins via isotopic studies, microwear patterns and craniodental correlates (see Teaford & Ungar, 2001
for a review). Incorporating cooked plants into
the hominin dietary repertoire, even after the
point when animal resources joined the menu,
may have allowed a much broader range of plant
species to be utilised (Leopold & Ardrey, 1972;
Alperson–Afil & Goren-Inbar, 2006; Gowlett,
2006) or, conversely, it might have increased reliance on a smaller range of plant foods.
Secondary compounds in plants, which
include digestion inhibitors and toxins, are found
in varying doses in many plants (Stahl, 1984). The
issue with these compounds is not in their presence per se, but in the dosage consumed, larger
doses causing more damage to the body or digestive process. Glander (1982) suggests that hominin dietary diversity offsets problems with secondary compounds by effectively diluting the amount
consumed such that they only had small or entirely
unnoticeable effects. Yet, cooking does often mitigate the effect of these compounds, opening up the
possibility that larger amounts of plants containing
them could be consumed than when raw, without
suffering any negative consequences. Inhibitors
act on digestion to reduce the amount of nutrients that can be adsorbed, while toxins have effects
elsewhere in the body. Digestion inhibitors often
impact on enzyme action. For example, trypsin
inhibitors reduce the action of this protein-digesting enzyme and are found in many plant foods
(Liener & Kakade, 1980). The protein structure
of inhibitors is mitigated by heat, which disrupts
their tertiary structure, making them inactive (e.g.
Privalov & Khechinashvili, 1974). Toxins such as
L. Attwell et al.
cyanogenic glycosides, glucosinolates, lathyrogens,
gossypol and antivitamins act on other parts of the
body, sometimes once they have been hydrolysed,
to cause problems in the nervous system, liver,
kidneys and, if the dose is large enough, they can
lead to death. The effects of these compounds are
also often mitigated if the food item is cooked
(Stahl, 1984).
The possible effects of reduced ingestion of
secondary compounds through cooking could
have influenced the digestive system by relaxing
the selection for dealing with such substances
(Wrangham, 1984). For example, the advantages
related to heightened sensitivity to xenobiotics
in plants, or a more efficient detoxification system, would have been relaxed as fire reduced the
need for systems to deal with these compounds
(Wrangham & Carmody, 2010). However, these
possible adaptive responses to reduced toxin
ingestion have not, to our knowledge, been studied from this evolutionary perspective.
Along with mitigating secondary compounds,
cooking may also “pre-digest” food (Milton,
2000), increasing digestibility and therefore
allowing more energy to be extracted for growth
and reproduction (Aiello & Key, 2002; Carmody
& Wrangham, 2009). This has been demonstrated in non-human mammals. For instance,
Nestares et al. (1996) found that rats gained more
weight on a diet of cooked versus raw chick peas,
and similarly Carmody et al. (2010) observed the
same phenomenon in mice eating cooked food
compared to those eating raw food. Plant foods,
though containing high levels of energy dense
polysaccharides, are often relatively difficult to
digest when raw. Cellulose, a polysacaride making up cell walls, is highly tough and fibrous, so is
not easily broken down by digestive enzymes and
may prevent enzyme access to other nutritious
compounds such as proteins. Humans are only
able to metabolise 0.6 - 2.1% of the raw cellulose
they consume (Southgate, 1973), because of the
relatively short digestive tract and lack of adaptive cellulose-digesting gut flora which assist with
this process in other mammal species. As a result,
plants are costly to digest, with cellulose making
up 33% of plant matter and only a small amount
11
of net energy gained from their consumption.
Many of the non-human primate species used
to model hominin behaviour preferentially eat
fruit and underground storage organs that contain less cellulose (Milton, 1980), suggesting the
early hominin diet may have been restricted in
a similar way. Cooking plants containing cellulose makes them much easier to digest, as heat
solubilises cellulose and breaks down its physical
structure (Lucas, 2011), allowing more energy to
be absorbed from the plant.
The energy value of cooked meat in comparison to raw meat is less clear than that for plants.
It has been suggested that cooking it increases
the energy that can be gained by denaturing proteins, making them easier to digest (Carmody
& Wrangham, 2009). Proteins, which comprise
a significant amount of animal matter in comparison to plants, are metabolically expensive to
digest, so cooking may increase the net energy
that can be gained, by reducing overall digestion
costs, an effect observed in captive snakes under
controlled conditions (Bobeck et al., 2007).
Cooking also reduces the structural integrity of
meat by denaturing the proteins that make up
collagen, which forms muscle fibres, thus making meat not only easier to digest but much easier to chew, so less time and energy is required
for mastication, similar to the effect of cooking some plant foods (Carmody et al., 2011b).
Cooking may also kill pathogens in meat, reducing the immune reaction costs of ingestion.
Cumulatively, all of these effects may allow more
energy to be diverted to the body for functions
other than digestion or immune reaction.
There are, however, aspects of cooking meat
which may reduce its energetic value. For example, fat is lost through dripping as it becomes
liquid when heated (Bender, 1992). Since fat
provides more calories per gram than protein,
its loss may significantly reduce the overall energetic value of meat. The method of cooking in
this regard is important though, with roasting
causing the greatest loss (Bender, 1992). The
Maillard reaction, in which amino acids combine with sugars to create a complex indigestible
structure, may also reduce the energy content
www.isita-org.com
12
Functions and consequences of hominin fire use
of meat when cooked (Maillard, 1916; Seiquer
et al., 2006). An experiment in mice did find
that cooked meat improved energy gain when
compared to raw meat (Carmody et al., 2011a)
but whether this effect is seen consistently in
humans, and for what methods of cooking,
needs to be evaluated in order to establish the
possible effect of cooked meat on hominin evolution. Currently the literature abounds with
food science studies evaluating this in modern,
processed goods for purposes of improving the
products or establishing links with diseases such
as cancer (e.g. Sinha et al., 1995; Dal Bosco et
al., 2001; Serrano et al., 2007), with little effort
directed towards wild resources or those simulating the animal resources that hominins procured
(but see Wandsnider, 1997; Speth, 2000).
It is possible that the extra energy that could
be gained from cooked food may have had an
effect on hominin morphological and physiological evolution. Aiello & Wheeler (1995) suggest
in their “Expensive Tissue Hypothesis” that the
brain expansion seen in H. ergaster around 1.5
mya, and then again in Middle Pleistocene Homo
around 0.5 mya, could only have occurred with
the reduction of another metabolically expensive
tissue, which they propose is the gut. They concluded the reduction of the gut would have been
necessary to reduce the energy it required overall, thus freeing up energy that could be directed
towards the brain. This theory suggests such a
reduction could only occur with the introduction of higher quality diet, possibly in the form
of carnivory or later, cooking.
In a more recent approach to this hypothesis
(Navarrete et al., 2011), no correlation between
digestive tract and brain size or between digestive tract and any other “expensive” organ across
mammals was found. However, brain size was
demonstrated to negatively correlate with adipose deposits (see Navarette et al., 2011, Fig. 2,
p. 92); the trade-off between brain size and the
amount of adipose tissue is hypothesised because
adipose is heavy and therefore expensive to carry
and maintain. By comparison to other primates,
humans in fact carry a significantly greater
amount of adipose, especially during infancy,
and less muscle, yet also have highly encephalised brains (Vasey & Walker, 2001; Leonard et
al., 2007; Snodgrass et al., 2009). Energy savings
would be required for this relationship to have
evolved. Amongst a suite of proposed behaviours and adaptions, locomotion is implicated.
Bipedalism is a more metabolically efficient
means of moving than other typical primate
modes such as arboreal quadrupedalism, suggesting that humans can support larger fat deposits
because it is less expensive to carry. The energy
that adipose stores provided was likely to be one
of the conditions that allowed the hominin brain
to become so large at a relatively lower metabolic
cost than in other species.
This renewed view of the “Expensive Tissue
Hypothesis” does not, however, entirely rule out
the importance of fire-induced dietary change.
Encephalisation to the extent seen in the already
bipedal early Homo would also have required
an increase in energy input, which may have
been provided through the consumption of
cooked food at this stage and again later during the Middle Pleistocene when evidence for
the control of fire and animal resource processing is more consistent and further brain enlargement occurred (Ben-Dor et al., 2011; Navarrete
et al., 2011). Increased cognitive buffering and
the ability to plan, cooperate and avoid starvation, are also likely to have unlocked the extra
energy input required to fuel hominin brain
expansion (Kaplan et al., 2000; Navarrete et al.,
2011). Similarly, cooperative breeding, which is
linked to food sharing, could have increased the
amount of energy hominins consumed whilst
also reducing the individual cost of gathering
food (Burkart et al., 2009). Thus, the cultural
transmission of fire may have contributed to the
genetic selective environment for brain size and
cognition, which then provided the capacity for
further invention to counteract variation in the
nutritional environment.
In addition to physiological and soft tissue
responses, cooking may have affected the selective environment for cranial and dental morphology, contributing to the reduced post canine
dentition of Homo erectus (Wood & Aiello,
L. Attwell et al.
1998), and comparatively small facial size of later
hominin species. Cooked food is much easier to
chew than raw, reducing masticatory strain and
selection for large molar teeth (Lieberman et
al., 2004). H. sapiens features, such as increased
salivary amylase to digest starches in the mouth,
reduced volume in the oral cavity, and a reduction
in jaw-muscle myosin (as less force is required to
chew softened food, see McCollum et al., 2006
for a brief summary of studies investigating the
genetic mechanism behind this), may also have
been influenced by consuming softened cooked
food (Lucas et al., 2006). Wrangham & ConklinBrittain (2003) use such morphological correlates to date the advent of cooking to 1.9 mya
and when H. ergaster may have eaten “the first
hot meal” (Wrangham et al., 1999). However,
the opposing view sees hominin cranio-dental
morphology at the time as being influenced
more greatly by the advent of carnivory through
scavenging raw animal resources of carcasses, a
major step change in and of itself. In this scenario the second rapid phase of encephalisation
seen in Middle Pleistocene Homo is due to cooking, indicating a later date for the evolution of
this behaviour and correlating more closely with
the archaeological record for controlled and consistent use of fire (e.g. Aiello & Wheeler, 1995).
Conclusions
We think it unlikely that there was a critical factor which “sparked” the unique trajectory
of hominin evolution towards modern human
morphology, behaviour and culture. However,
it is clear that the harnessing of commonly experienced natural fires and the social transmission
of fire creation and maintenance technology
had the potential to play an important role in
both cultural and genetic evolutionary dynamics within the Plio-Pleistocene hominin lineage.
Determining when this occurred relies on an
understanding of the residual effects of fire in the
archaeological record, but we must also contend
with the likelihood that the earliest phases of fire
use were too ephemeral to leave clearly detectable
13
traces. Although earlier examples are debated in
the African record, evidence for the consistent
use of fire emerges in the Middle Pleistocene at
hominin sites such as Gesher Benot Ya’aqov in
the Middle East. It spreads eventually and probably during successive events to Asia, Europe and
Africa. Zhoukoudian in China provides the most
compelling evidence for the independent evolution of fire use behaviour outside of the Middle
East during this early stage. Fire is visible in
Europe somewhat later in time and long after the
initial arrival of Homo, raising questions about its
necessity in hominin survival.
There are numerous ways in which the use of
fire may have impacted upon hominin evolution,
with light and heat being the two primary “drivers”. As we have reviewed, light allows the active
part of the day to continue into the night and
heat is used to process animal and non-animal
resources. Both light and heat may facilitate the
exploration of and migration into cooler, northerly regions and are clearly contributors to the
social function that fire has in bringing groups
together for security and socialisation, as well
as keeping predators at bay. The consequences
stimulated by such fire-related behaviours are
commonly hypothesised to be biological/physiological, such as in the light that enters the eye
and the subsequent hormonal cascade which may
have impacted upon sleep cycles and reproductive timing, or the consumption of cooked foods
providing increased energy diverted towards
encephalisation and concomitant evolution of
craniodental morphology relating to the mastication of new foodstuffs. We have also emphasised the possible cultural evolutionary effects of
fire use and co-evolutionary scenarios such as the
way that individuals were brought together into
potentially larger groups interacting with each
other around a central fire source and the relationship between this social scenario and increasing brain size and cognitive complexity.
The hominin fossil and archaeological
records provide sources of information regarding evidence for fire use in the Plio-Pleistocene
and the evolutionary consequences of this
behaviour. Future work should seek to develop
www.isita-org.com
14
Functions and consequences of hominin fire use
a biogeographical picture of the evolution of fire
use, as well as an explanation for the long gaps in
time that occur in between the first few observable traces of fire and its widespread, intentional use (be this a consequence of genuinely
limited use in the initial stages or taphonomy).
Additionally, research should focus on setting the
use of fire in a palaeoecological context to test
hypotheses of dispersal and niche construction.
Many of the more nuanced physiological effects
may be difficult to detect in the past and pursuing a line of enquiry that includes determining
how firelight and heat impact on extant mammals, especially non-human primates and modern humans in different ecological and cultural
settings, will assist in substantiating some of the
current hypotheses and determining the extent
which the effects had a significant influence on
the evolution of the global, social species that we
are today.
Acknowledgements
We thank the Department of Anthropology, Durham University, for financial support to LA for this
collaboration following her graduation from the
undergraduate programme. We also thank colleagues
and two reviewers for their insightful comments.
References
Aiello L. C. & Wheeler P. 1995. The expensive
tissue hypothesis: the brain and the digestive
system in human and primate evolution. Curr.
Anthropol., 36: 199-221.
Aiello L.C. & Key C. 2002. Energetic consequences of being a Homo erectus female. Am. J.
Hum. Bio., 14: 551–565.
Alperson-Afil N. & Goren-Inbar N. 2006. Out
of Africa and into Eurasia with controlled use
of fire: evidence from Gesher Benot Ya’aqov,
Israel. Archaeology, Ethnology and Anthropology
of Eurasia, 4: 63–78.
Alperson-Afil N., Richter D. & Goren-Inbar N.
2007. Phantom hearths and the use of fire at
Gesher Benot Ya’aqov, Israel. PaleoAnthropology,
2007: 1-15.
Alperson-Afil N. & Goren-Inbar N. 2010. The
Acheulian Site of Gesher Benot Ya’aqov, vol.
II: Ancient Flames and Controlled Use of Fire.
Springer, Dordrecht.
Archibald S., Staver A. C. &Levin S. A. 2012.
Evolution of human-driven fire regimes in
Africa. Proc. Natl. Acad. Sci. U.S.A., 109:
847-852.
Arzarello M., Marcolini F., Pavia G., Pavia M.,
Petronio C., Petrucci M., Rook L. & Sardella
R. 2007. Evidence of earliest human occurrence
in Europe: the site of Pirro Nord (Southern
Italy). Naturwissenschaften, 94: 107–112.
Barbetti M., Clark J. D., Williams F. M. &
Williams M. A. G. 1980. Palaeomagnetism and
the search for very early fireplaces: results from
a million year old Acheulian site in Ethiopia.
Anthropologie, 18: 299-304.
Beaumont P. B. 2011. The edge: More on fire
making by about 1.7 million years ago at
Wonderwerk Cave in South Africa. Curr.
Anthropol., 52: 585-595.
Bellomo R. V. 1991. Identifying traces of natural
and humanly controlled fire in the archaeological record: the role of actualistic studies.
Archaeology in Montana, 32:75-93.
Bellomo R.V. 1993. A methodological approach
for identifying archaeological evidence of fire
resulting from human activities. J. Arch. Sci.,
20: 525-553.
Bellomo R.V. 1994. Methods of determining
early hominid behavioural activities associated
with the controlled use of fire at FxJj 20 Main.
Koobi Fora, Kenya. J. Hum. Evol., 27: 173-195.
Bellomo R.V. & Kean W.F. 1994. Evidence of
hominid-controlled fire at the FxJj 20 Site
Complex, Karari Escarpment, Koobi Fora,
Kenya. In G. L. Isaac & B. Isaac (eds): Koobi
Fora Research Project Monograph Series Volume
3: Archaeology. Clarendon Press, Oxford, UK.
Ben-Dor M., Gopher A., Hershkovitz I. & Barkai
R. 2011. Man the fat hunter: the demise of
Homo erectus and the emergence of a new hominin lineage in the Middle Pleistocene (ca. 400
kyr) Levant. PLoS ONE, 6: e28689.
L. Attwell et al.
Bender A. 1992. Meat and Meat Products in
Human Nutrition in Developing Countries.
Food and Agriculture Organization of the
United Nations. Food and Nutrition Paper
No. 53.
Berna F., Goldberg P., Horwitz L.K., Brink J.,
Holt S., Bamford M. & Chazan M. 2012.
Microstratigraphic evidence of in situ fire in
the Acheulean strata of Wonderwerk Cave,
Northern Cape province, South Africa. Proc.
Natl. Acad. Sci. U.S.A.,109: e1215-e1220.
Boback S.M., Cox C.L., Ott B.D., Carmody R.,
Wrangham R.W. & Secor S.M. 2007. Cooking
and grinding reduces the cost of meat digestion.
Comp. Biochem. Physiol., Part A: Mol. Integr.
Physiol., 148: 651-656.
Bobe R. 2006. The evolution of arid ecosystems
in eastern Africa. J. Arid Environ. 66: 564-584.
Bond W.J., Woodward F.I. & Midgley G.F. 2005.
The global distribution of ecosystems in a world
without fire. New Phytol., 165: 525-538.
Bond W. J. & Keeley J. E. 2005. Fire as a global ‘herbivore’: the ecology and evolution of
flammable ecosystems. Trends Ecol. Evol., 20:
387-394.
Brace C.L. 1999. An anthropological perspective
on ‘race’ and intelligence: the non-clinical nature on human cognitive abilities. J. Anth. Res.,
55: 245-264.
Brain C.K. & Sillen A. 1988. Evidence from
the Swartkrans cave for the earliest use of fire.
Nature, 336: 464.
Brainard S.M., Hanifin J., Gresson J., Byrne B.,
Glickman G., Gerner E. & Rollag D. 2001
Action spectrum for melatonin regulation in
humans: evidence for a novel circadian photoreceptor. J. Neuro., 21: 6405-6412.
Brockman D.K. 2005. What do studies of seasonality in primates tell us about human evolution? In D. K. Brockman & C. van Schaik (eds):
Seasonality in primates: Studies of living and extinct
human and nonhuman primates, pp.543-571.
Cambridge University Press, Cambridge, UK.
Brown F. H. 1994. Development of Pliocene and
Pleistocene chronology of the Turkana Basin,
East Africa and its relation to other sites. In R.
S. Corruccini & R. L. Ciochon (eds): Integrative
15
Paths to the Past, pp. 285-312. Prentice-Hall,
Englewood Cliffs, NJ.
Burkart J. M., Hrdy S. B. & van Schaik C. P.
2009. Cooperative breeding and human cognitive evolution. Evol. Anthropol., 18: 175-186.
Burton F.D. 2009. Fire: The spark that ignited human evolution. University of New Mexico Press,
Albuquerque, USA.
Cajochen C., Krauchi K. & Wirz A. 2003. Role
of Melatonin in the regulation of human circadian rhythms and sleep. J. Neuroendocrinol.,
15: 432-437.
Carbonell E., Bermúdez de Castro J.M., Parés
J.M., Pérez-González A., Cuenca-Bescós G.,
Ollé A., Mosquera M., Huguet R., van der
Made J., Rosas A., Sala R,. Vallverdú J., García
N., Granger D.E., Martinón-Torres M.,
Rodríguez X.P., Stock G.M., Vergès J.M., Allué
E., Burjachs F., Cáceres I., Canals A., Benito A.,
Díez C,. Lozano M., Mateos A., Navazo M.,
Rodríguez J., Rosell J. & Arsuaga J.L. 2008.
The first hominin of Europe. Nature, 452:
465-469.
Carbonell E., Garcia-Anton M.D., Mallol
C., Mosquera M., Olle A., Rodriguez X.P.,
Sahnouni M., Sala R., Verges J.M. 1999. The
TD6 level lithic industry from Gran Dolina,
Atapuerca (Burgos, Spain): production and use.
J. Hum. Evol., 37: 653–693.
Carmody R.N., Weintraub G.S., Secor S.M. &
Wrangham R.W. 2010. Energetic significance
of food processing: a test of the cooking hypothesis. Integr. Comp. Biol., 50:e24.
Carmody R.N. & Wrangham R.W. 2009. The energetic significance of cooking. J. Hum. Evol.,
57: 379-391.
Carmody R.N., Weintraub G.S. & Wrangham
R.W. 2011a. Energetic consequences of thermal and nonthermal food processing. Proc.
Natl. Acad. Sci. U.S.A., 108: 19199-19203.
Carmody R.N., Weintraub G.S. & Wrangham
R.W. 2011b. More valuable meat: energetic
effects of cooking on a key hominin resource.
Am. J. Phys. Anthropol., 144:105.
Cashmore A. 2003. Cryptochromes: Enabling
plants and animals to determine circadian time.
Cell, 144: 537-543.
www.isita-org.com
16
Functions and consequences of hominin fire use
Chazan M., Ron H., Matnon A., Porat N.,
Goldberg P., Yates R., Avery M., Sumner A.,
Horwitz L.K. 2008. Radiometric dating of the
Earlier Stone Age sequence in Excavation I at
Wonderwerk Cave, South Africa: preliminary
results. J. Hum. Evol., 55: 1-11.
Clark J. D. 1987. Transitions Homo erectus and
the Acheulian: the Ethiopian sites of Gadeb and
the Middle Awash. J. Hum. Evol., 16: 809-826.
Clark J. D. & Harris J. W. K. 1985. Fire and
its roles in early hominid lifeways. African
Archaeological Review, 3: 3-27.
Dal Bosco A., Castellini C. & Bernardini M.
2001. Nutritional quality of rabbit meat as
affected by cooking procedure and dietary
Vitamin E. J. Food Sci., 7: 1047-1051.
Doran D.M. 1997. Influence of seasonality on activity patterns, feeding behaviour, ranging and
grouping patterns in Tai chimpanzees. Int. J.
Primatol., 18: 183-206.
Dumont M. & Beaulieu C. 2007. Light exposure
in the natural environment: relevance to mood
and sleep disorders. Sleep Med., 8: 557-565.
Dunbar R. I. M. 1998. The social brain hypothesis. Evol. Anthropol., 6: 178–190.
Finch C.E. & Stanford C.B. 2004. Meat-adaptive
genes and the evolution of slower aging in humans. Q. Rev. Biol., 79: 3-50.
Gambles C. 1999. The Palaeolithic societies of Europe. Cambridge University Press,
Cambridge, UK.
Gichohi H., Gahaku C., & Mwangi E. 1996.
Savanna ecosystems. In T.R. McClanahan &
T.P. Young (eds): East African Conservation
Systems and their Conservation, pp. 273-298.
Oxford University Press, Oxford.
Glander K. E. 1982. The impact of plant secondary compounds on primate feeding behaviour.
Yearb. Phys. Anthropol., 25:1-18.
Glatstone A.R.H. 1979. Reproduction and behaviour of the lesser mouse lemur (Microcebus
murinus, Milton 1777) in captivity. PhD thesis,
University of London, University College.
Goldman B. 2001. Mammalian photoperiodic
system: Formal properties and neuroendocrine
mechanisms of photoperiodic time measurement. J. Bio. Rhythms, 18: 71-79.
Goldman B. D. 2003. Pattern of melatonin secretion mediates transfer of photoperiod information from mother to fetus in mammals. Sci.
STKE,192: pe29.
Goren-Inbar N., Alperson N., Kislev M.E.,
Simchoni O., Melamed Y., Ben-Nun A. &
Werker E. 2004. Evidence of hominin control
of fire at Gesher Benot Ya’aqov, Israel. Science,
304: 725-727.
Goren-Inbar N., Feibel C. S., Verosub K. L.,
Melamed V., Kislev M. E., Tchernov E. &
Saragusti I. 2000. Pleistocene milestones on the
out-of-Africa corridor at Gesher Benot Ya’aqov,
Israel. Science, 289: 944-947.
Goren-Inbar N., Sharon G., Melamed Y. & Kislev
M. 2002. Nuts, nut cracking, and pitted stones
Gesher Benot Ya‘aqov, Israel. Proc. Natl. Acad.
Sci. U.S.A, 99: 2455-2460.
Gorman M.R. & Lee T.M. 2002. Hormones
and biological rhythms. In J.B. Becker, S.M.
Breedlove, D. Crews & M.M. McCarthy
(eds): Behavioural endocrinology. MIT Press,
Cambridge, MA.
Gowlett J.A.J., Harris J.W.K., Walton D. & Wood
B.A. 1981. Early archaeological sites hominid
remains and traces of fire from Chesowanja,
Kenya. Nature, 294: 125-129.
Gowlett J.A.J. 2006. The early settlement of
northern Europe: Fire history in the context
of climate change and the social brain. C. R.
Palevol., 5: 299-310.
Gowlett J.A.J. 2001 Archaeology: out in the cold.
Nature, 413: 33-34.
Grossman E. Laudon M., Yalcin R., Zengil H.,
Peleg E., Sharabi Y., Kamari Y., Shen-Orr Z.
& Zisapel N. 2006. Melatonin reduces night
blood pressure in patients with nocturnal hypertension. Am. J. Med., 10: 898-902.
Grossman E. Laudon & Zisapel N. 2011. Effect
of melatonin on nocturnal blood pressure: meta-analysis of randomized controlled trials. Vasc.
Health Risk Manag., 7: 577-584.
Harris J. W. K. 1978. The Karari Industry: Its
Place in East African Prehistory. PhD Thesis,
University of California, Berkeley.
Higham T., DoukaK., Wood R., Ramsey C.B.,
Brock F., Basell L., Camps M., Arrizabalaga
L. Attwell et al.
A., Baena J., Barroso-Ruíz C., Bergman C.,
Boitard C., Boscato P., Caparrós M., Conard
N.J., Draily C., Froment A., Galván B.,
Gambassini P., Garcia-Moreno A., Grimaldi
S., Haesaerts P., Holt B., Iriarte-Chiapusso M.,
Jelinek A., Jordá Pardo J.F., Maíllo-Fernández
J., Marom A., Maroto J., Menéndez M.,
Metz L., Morin E., Moroni A., Negrino F.,
Panagopoulou E., Peresani M., Pirson S., de
la Rasilla M., Riel-Salvatore J., Ronchitelli A.,
Santamaria D., Semal P., Slimak L., Soler J.,
Soler N., Villaluenga A., Pinhasi R. & Jacobi
R. The timing and spatiotemporal patterning
of Neanderthal disappearance. Nature, 512:
306-309.
Huang L., Zhang C., Hou Y., Laudon M., She
M., Yang S., Ding L., Wang H., Wang Z., He P.
& Yin W. 2013. Blood pressure reducing effects
of piromelatine and melatonin in spontaneously hypertensive rats. Eur. Rev. Med. Pharmacol.
Sci., 17: 2449-56.
Jacobs B.F. 2004. Palaeobotanical studies from
tropical Africa: relevance to the evolution of
forest, woodland and savannah biomes. Phil.
Trans. Roy. Soc. B., 359: 1573–1583.
Kaplan H., Hill K., Lancaster J. & Hurtado A.
M. 2000. A theory of human life history evolution: diet, intelligence, and longevity. Evol.
Anthropol., 9: 156-185.
Karkanas P., Shahack-Gross R., Ayalon A., BarMatthews M., Barkai R., Frumkin A., Gopher
A. & Stiner M.C. 2007. Evidence for habitual
use of fire at the end of the Lower Paleolithic:
Site-formation processes at Qesem Cave, Israel
J. Hum. Evol., 53: 197-212.
Kerr B., Schwilk D.W., Bergman A. & Feldman
M.W. 1999. Rekindling an old flame: A haploid model for the evolution and impact of
flammability in resprouting plants. Evol. Ecol.
Res., 1: 807-833.
Kuller R. 2002. The influence of light on circadian rhythms in humans. J. Physiol. Anthrop.
App. Hum. Sci., 21: 87-91.
Leonard W.R., Snodgrass J.J. & Robertson M.L.
2007. Effects of brain evolution on human nutrition and metabolism. Annu. Rev. Nut., 27:
311-327.
17
Leopold A.C. & Ardrey R. 1972. Toxic substances in plants and the food habits of early man.
Science, 176: 512-514.
Lieberman D.E., Krovitz G.E., Yates F.W., Devlin
M. & Claire M.S. 2004. Effects of food processing on masticatory craniofacial growth in a
retrognathic face. J. Hum. Evol., 146: 655-677.
Liener I.E. & Kakade M.L. 1980. Protease inhibitors. In I.E.Liener (ed): Toxic constituents of plant
foodstuffs, pp. 7-71. Academic Press, New York.
Lindburgh D.G. 1987. Seasonality of reproduction in priamtes. In G. Mitchell & J. Erwin
(eds): Comparative Primate Biology, Vol 2B:
Behavior, Cognition and Motivation, pp. 167218. Alan R. Liss, New York.
Lockley S.W., Brainard G.C. & Czeisler C.A.
2003. High sensitivity of the human circadian
melatonin rhythm to resetting by short wavelength light. J. Clini. Endocri. Metab., 88:
4502-4505.
Gabunia L., Vekua A., Lordkipanidze D., Swisher
III C.C., Ferring R., Justus A., Nioradze M.,
Tvalchrelidze M., Anton S.C., Bosinski G.,
Joris O., de Lumley M.A., Majsuradze G. &
Mouskhelishvili A. 2000. Earliest Pleistocene
Hominid Cranial Remains from Dmanisi,
Republic of Georgia: Taxonomy, Geological
Setting, and Age. Science, 288: 1019-1025.
Lucas P.W. 2011. Cooking clue to human dietary
diversity. Proc. Natl. Acad. Sci. U.S.A., 108:
19101-19102.
Lucas P.W., Ang K.Y., Sui Z., Agrawal K.R., Prinz
J.F. & Dominy N.J. 2006. A brief review of the
recent evolution of the human mouth in physiological and nutritional contexts. Physio. Behav.,
89: 36-38.
McCollum M.A., Sherwood C.C., Vinyard C.J.,
Lovejoy C.O. & Schachat F. 2006. Of musclebound crania and human brain evolution: The
story behind the MYH16 headlines. J. Hum.
Evol., 50: 232-236.
Maillard L.C. 1916. A synthesis of humic matter by effect of amine acids on sugar reducing
agents. Annales de Chimie, 5: 258–316.
Mania D. & Mania U. 2005. The natural and
socio-cultural environment of Homo erectus at
Bilzingsleben, Germany. In C.S. Gamble & M.
www.isita-org.com
18
Functions and consequences of hominin fire use
Porr (eds): The Hominid Individual in Context:
Archaeological Investigations of Lower and Middle
Palaeolithic Landscapes, Locales and Artefacts, pp.
98–114. Routledge, London.
Menault J-C. 1983. The vegetation of African
savannas. In F. Boulière (ed): Ecosystems of the
World: Tropical Savannas, pp. 109-149. Elsevier,
Amsterdam.
Mercier N., Froget L., Miallier D., Pilleyre T.,
Sanzelle S. & Tribolo C. 2004. Nouvelles données chronologiques pour le site of MenezDregan 1 (Bretagne): l’apport de la thermoluminescence. Quaternaire, 15: 253–61.
Milton K. 1980. The foraging strategy of howler
monkeys. Columbia University Press, New York.
Milton K. 2000. Hunter-gatherer diets: a different
perspective. Am. J. Clini. Nutr., 71: 665-667.
Morley R.J. & Richards K. 1993. Gramineae
cuticle: a key indicator of Late Cenozoic climatic change in the Niger Delta. Rev. Palaeobot.
Palyno., 77: 119-127.
Nestares T., López-Frías M., Barrionuevo M. &
Urbano G. 1996. Nutritional assessment of raw
and processed chickpea (Cicer arietinum L.)
protein in growing rats. J. Agric. Food Chem.,
44: 2760–2765.
Olcese J., Lozier S. & Paradise C. 2013. Melatonin
and the circadian timing of human parturition.
Reprod. Sci., 20: 168-174.
Paulis L. & Simko F. 2007. Blood pressure modulation and cardiovascular protection by melatonin: potential mechanisms behind. Physiol.
Res., 56: 671-684.
Pausas J. G. & Keeley J. E. 2009. A Burning Story:
The role of fire in the history of life. BioScience,
59: 593-601.
Peris J. F., González V. B., Blasco R., Cuartero F.,
Fluck H., Sañudo P. & Verdasco C. 2012. The
earliest evidence of hearths in southern Europe:
the case of Bolomor Cave (Valencia, Spain).
Quatern. Int., 247: 267–77.
Pickering T. 2001. Taphonomy of the Swartkrans
hominid postcrania and its bearing on issues
of meat-eating and fire management. In C.B.
Stanford & H.T. Bunn (eds): Meat Eating
and Human Evolution, pp. 332-349. Oxford
University Press, Oxford.
Preece R.C., Gowlett J.A.J., Parfitt S.A.,
Bridgland D.R. & Lewis S.G. 2006. Humans
in the hownian: habitat, context and fire use at
Beeches Pit, West Stow, Suffolk, UK. J. Quater.
Sci., 21: 485-496.
Preece R. C., Parfitt S. A., Bridgland D. R.,Lewis
S. G., Rowe P. J., Atkinson T. C., Candy
I., Debenham N. C., Penkman K. E. H.,
Rhodes E. J., Schwenninger J. L., Griffiths
H. I., Whittaker J. E. & Gleed-Owen C.
2007. Terrestrial environments during MIS
11: evidence from the Palaeolithic site at West
Stow, Suffolk, UK. Quaternary. Sci. Rev., 26:
1236-1300.
Pruetz J. D. & LaDuke T.C. 2010. Brief
Communication: Reaction to Fire by Savanna
Chimpanzees (Pan troglodytes verus) at
Fongoli,Senegal: Conceptualization of ‘‘Fire
Behavior’’ and the Case for a Chimpanzee
Model. Am. J. Phys. Anthrpol., 141: 646–650
Privalov P.L. & Khechinashvili N.N. 1974. A
thermodynamic approach to the problem of
stabilization of globular protein structure: A
calorimetric study. J. Mol. Biol. 86: 665-684.
Raloff J. 1998. Does light have a dark side? Nighttime illumination might elevate cancer risk.
Science news online, 154: 1-7.
Reid K. J,& Zee P. C. 2005. Circadian disorders of the sleep–wake cycle. In Kryger M.H.,
Roth T. & Dement W.C. (eds): Principles and
practice of sleep medicine, pp. 691–701. Elsevier
Saunders, Philadelphia.
Richerson P.J., Boyd R. & Henrich J. 2010.
Colloquium paper: gene-culture coevolution
in the age of genomics. Proc. Natl. Acad. Sci.
U.S.A., 107: 8985.
Richter D. 2008. Altersbestimmung der
Fundschichten von Schöningen mit dosimetrischen Datierungsmethoden In H. Thieme
& R. Maier (eds): Die Schöninger Speere—
Mensch und Jagd vor 400,000 Jahren, pp. 62–
66. Konrad Theiss, Stuttgart, Germany.
Roebroeks W. & Villa P. 2011. On the earliest evidence for habitual fire use in Europe. Proc. Natl.
Acad. Sci. U.S.A., 108: 5209-5214.
Rolland N. 2004. Was the emergence of home
bases and domestic fire a punctuated event?
L. Attwell et al.
A review of the middle Pleistocene record in
Eurasia. Asian Perspectives, 43: 248-280.
Rosenthal N. E., Sack D.A., Gillin J.C., Lewy
A. J., Goodwin F. K., Davenport Y., Mueller
P. S., Newsome D.A. & Wehr T. A. 1984.
Seasonal affective disorder- a description of the
syndrome and preliminary findings with light
therapy. Arch. Gen. Psychiatry, 41: 72-80.
Toups M.A., Kitchen A., Light, J.E. & Reed D.L.
2011. Origin of clothing lice indicates early
clothing use by anatomically modern humans
in Africa. Mol. Biol. Evol., 28: 29-32.
Sancar A. .2000. Cryptochrome: The second photoactive pigment in the eye and role in circadian photoreception. Ann. Revi. Biochem., 69:
31-67.
Sancar A. 2004. Regulation of the mammalian circadian clock by cryptochrome. J. Biol. Chem.,
279: 34079-34082.
Scott A. C. 2000. The pre-quaternary history of
fire. Palaeogeo. Palaeoclimatol. Palaeoecol., 164:
297–345
Seiquer I., Diaz-Alguacil J., Delgado-Andrade
C., Lopez-Frias M., Hoyos A.M., Galdo G.
& Navarro M.P. 2006. Diets rich in Maillard
reaction products affect protein digestibility in
adolescent males aged 11–14 y. Am. J. Clinic.
Nutrition, 83:1082–1088.
Serrano A., Librelotto J., Cofrades S., SánchezMuniz F.J. & Jiménez-Colmenero F. 2007.
Composition and physicochemical characteristics of restructured beef steaks containing walnuts as affected by cooking method. Meat Sci.,
77: 304-313.
Shultz S., Nelson E. & Dunbar R. I. M. 2012.
Hominin cognitive evolution: identifying patterns and processes in the fossil and archaeological record. Phil. Trans. R. Soc. B., 367:
2130-2140.
Sinha R., Rothman N., Brown E.D., Salmon
C.P., Knize M.G., Swanson C.A., Rossi S.C.,
Mark S.D., Levander O.A. & Felton J.S.
1995. High concentrations of the carcinogen
2-Amino-1-methyl-6-phenylimidazo-[4,5-b]
pyridine (PhIP) occur in chicken but are dependent on the cooking method. Cancer Res.,
55: 4516-4519.
19
Snodgrass J.J., Leonard W.R. & Robertson
M.L. 2009. The energetics of encephalisation in early hominids. In J-J. Hublin & M.J.
Richards (eds): The Evolution of Hominin Diets:
Integrating Approaches to the Study of Palaeolithic
Subsistence, pp. 15–29. Springer Science and
Business Media B.V., London.
Southgate D.A.T. 1973. Fibre and the other
available carbohydrates and their effects on
the energy value of the diet. Proc. Nutr. Soc.,
32:131-136.
Speth J.D. 2001. Boiling vs. baking and roasting:
a taphonomic approach to the recognition of
cooking techniques in small mammals. In P.A.
Rowley-Conwy (ed): Animal Bones, Human
Societies, pp. 89-105. Oxbow Books, Oxford.
Stahl A.B. 1984. Hominid dietary selection before
fire. Curr. Anthropol., 25: 151-168.
Stehle J. H., Von Gall C. & Korf H. W. 2003.
Melatonin: A clock output, a clock input. J.
Neuroendocrinol., 15: 383-389.
Teaford M.F. & Ungar P.S. 2001. Diet and the
evolution of the earliest hominin ancestors.
Proc. Natl. Acad. Sci. U.S.A., 97: 13506-13511.
Thevenon F., Williamson D., Bard E., Anselmetti F.
S., Beaufort L. & Cachier H. 2010. Combining
charcoal and elemental black carbon analysis
in sedimentary archives: Implications for past
fire regimes, the pyrogenic carbon cycle, and
the human–climate interactions. Global Planet
Change, 72: 381–389.
Thieme H., 2005. The Lower Palaeolithic art
of hunting: the case of Schöningen 13 II-4,
Lower Saxony, Germany. In C. Gamble & M.
Porr (eds): The Hominid Individual in Context:
Archaeological Investigations of Lower and Middle
Palaeolithic Landscapes, Locales and Artefacts,
pp.115–32. Routledge, London.
Tsantarliotou M.P. & Taitzoglou I.A. 2012.
Melatonin effect on reproduction. In R.R Watson
(ed): Melatonin in the Promotion of Health, pp.
115-129. CRC Press, Boca Raton, FL.
Vasey N. & Walker A. 2001. Neonate body size
and hominid carnivory. In C.B. Stanford &
H.T. Bunn (eds): Meat Eating and Human
Evolution, pp. 332-349. Oxford University
Press, Oxford.
www.isita-org.com
20
Functions and consequences of hominin fire use
Wandsnider L. 1997. The roasted and the boiled:
food composition and heat treatment with
special emphasis on pit-hearth cooking. J.
Anthropol. Archaeol., 16: 1–48.
Wallis J.1995. Seasonal influence on reproduction
in chimpanzees of Gombe National Park. Int. J.
Primatol.,16: 435-451.
Wallis J.1997. A survey of reproductive parameters in the free-ranging chimpanzees of Gombe
National Park. J.Reprod.Fertil.,109: 297-307.
Wehr T.A. 2001. Photoperiodism in humans and
other primates: evidence and implications. J.
Biol. Rhythms, 16: 348-364.
Wehr T. A., Duncan Jr. W. C., Sher L, Aeschbach
D., Schwartz P.J., Turner E. H., Postolache T.
T. & Rosenthal N. E. 2001. A circadian signal
of change of season in patients with seasonal
affective disorder. Arch. Gen. Psychiatry, 58:
1108–14.
Weiner S., Xu Q. Q.,Goldberg P., Liu J. & BarYosef O. 1998. Evidence for the use of fire at
Zhoukoudian. Science, 281: 251-253.
Wilson M. E., Gordon T. P., Rudman C.R. &
Tanner J. M. 1988. Effects of a natural versus
artificial environment on the tempo of maturation in female rhesus monkeys. Endocrinology,
12: 2653 -2661.
Wilson M. E. & Gordon T. P. 1989a. Season
determines timing of first ovulation in
outdoor-housed rhesus monkeys. J. Reprod.
Fertil., 85: 583 591.
Wilson M. E. & Gordon T. P. 1989b. Short-day
melatonin pattern advances puberty in seasonally breeding rhesus monkeys. J. Reprod. Fertil.,
86: 435-444.
Wood B. & Aiello L.C. 1998. Taxonomic and functional implications of mandibular scaling in early
hominins. Am. J. Phys. Anthrpol., 105: 523–538.
Wrangham R. & Carmody R. 2010. Human adaptation to the control of fire. Evol. Anthropol.,
19: 187-199.
Wrangham R. & Conklin-Brittain N. 2003.
Cooking as a biological trait. Comp. Biochem.
Physio. Part A, 136: 35-46.
Wrangham R.W., Jones J.H., Laden G., Pilbeam
D. & Conklin-Brittain N.L. 1999. The raw
and the stolen: cooking and the ecology of human origins. Curr. Anthropol., 40: 567-594.
Wrangham R.W. 1984. Comment on Stahl
(1984) Hominid dietary selection before fire.
Curr. Anthropol., 25: 151-168.
Young S. M., Benyshek D. C. & Lienard P. 2012.
The conspicuous absence of placenta consumption in human postpartum females: the fire hypothesis. Ecol. Food. Nutr., 51: 198-217.
Editor, Giovanni Destro Bisol
This work is distributed under the terms of a Creative Commons Attribution-NonCommercial 4.0
Unported License http://creativecommons.org/licenses/by-nc/4.0/